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Flowering Phenology As a Functional Trait in a Tallgrass Prairie

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Flowering Phenology As a Functional Trait in a Tallgrass Prairie Research Flowering phenology as a functional trait in a tallgrass prairie Joseph M. Craine1, Elizabeth M. Wolkovich2, E. Gene Towne1 and Steven W. Kembel3 1Division of Biology, Kansas State University, Manhattan, KS 66502, USA; 2Ecology, Behavior & Evolution Section, University of California, San Diego, 9500 Gilman Drive #0116, La Jolla, CA 92093,USA; 3Center for Ecology & Evolutionary Biology, University of Oregon, Eugene, OR 97403, USA Summary Author for correspondence: • The timing of flowering is a critical component of the ecology of plants and has the poten- Joseph M. Craine tial to structure plant communities. Yet, we know little about how the timing of flowering Tel: +1 785 532 3062 relates to other functional traits, species abundance, and average environmental conditions. Email: [email protected] • Here, we assessed first flowering dates (FFDs) in a North American tallgrass prairie (Konza Received: 18 August 2011 Prairie) for 431 herbaceous species and compared them with a series of other functional traits, Accepted: 29 September 2011 environmental metrics, and species abundance across ecological contrasts. • The pattern of FFDs among the species of the Konza grassland was shaped by local climate, New Phytologist (2011) can be linked to resource use by species, and patterns of species abundance across the land- doi: 10.1111/j.1469-8137.2011.03953.x scape. Peak FFD for the community occurred when soils were typically both warm and wet, while relatively few species began flowering when soils tended to be the driest. Compared with late-flowering species, species that flowered early had lower leaf tissue density and were Key words: climate, community assembly, drought, grass, Konza Prairie. more abundant on uplands than lowlands. • Flowering phenology can contribute to the structuring of grassland communities, but was largely independent of most functional traits. Therefore, selection for flowering phenology may be independent of general resource strategies. Introduction If the timing of flowering is an important component of com- munity assembly, there should be general rules that pattern varia- The timing of flowering is a critical component of the ecology of tion in flowering for a community (Armbruster et al., 1994; plants and can be an important component of community assem- Morales et al., 2005; Elzinga et al., 2007). If flowering time is bly as flowering phenology influences not only the relative abun- neutral within a growing season and uninfluenced by species dance of species in a given ecosystem, but also their presence or interactions and environmental conditions within the growing absence (Rathcke & Lacey, 1985; Sargent & Ackerly, 2008; season then a null-model such as the mid-domain hypothesis Crimmins et al., 2011). One manner in which flowering phenol- (Morales et al., 2005) may accurately predict the pattern of flow- ogy affects the composition of plant communities is through its ering phenology at the community level. The mid-domain effect on species interactions. Overlap of flowering times among hypothesis predicts that flowering for a flora should be greatest in species is almost inevitable in most communities, generating the the middle of the growing season as a consequence of the potential for strong competition, but also facilitation, for pollina- constraints of species placement in a bounded growing season tion resources (Rathcke & Lacey, 1985). Independent of pollina- (Morales et al., 2005). If flowering time, however, is critical to tion, flowering phenology indirectly affects species interactions, competition for pollinators and other resources (Kochmer & as flowering times may be associated with other aspects of perfor- Handel, 1986; Rathcke, 1988; Godoy et al., 2009) or avoidance mance, such as canopy development (Cleland et al., 2006), that of environmental stress (Reich & Borchert, 1984; Penuelas et al., influence competition for resources required for vegetative 2004), patterns may deviate from null model expectations. For growth. While many temperate woody species flower before example, in many grasslands, soil moisture stress can strongly leaves are produced, most temperate grassland species flower at limit plant production and reproduction. Even in grasslands the time of maximum vegetative biomass (Mooney et al., 1986; where growing season length is dictated by temperatures, soil Sun & Frelich, 2011), causing species with similar flowering moisture stress can be high in the middle of the growing season times to also compete for limiting soil resources and ⁄ or light. as leaf area develops, temperatures peak, precipitation declines, Flowering phenology can also influence plant success indepen- and soil moisture is depleted (Briggs & Knapp, 1995; Nippert dently of species interactions. Flowering when environmental et al., 2006; Craine et al., 2010). In such grasslands, midsummer stress is typically high, such as when temperatures are frequently soil moisture stress in many grasslands is frequent even in years cold or soil moisture is typically low, can also lower plant fecun- with above-average precipitation (Nippert et al., 2011). dity if not lead to the species’ local extirpation (Lacey et al., If flowering time for a species influences its exposure to envi- 2003; Inouye, 2008). ronmentally stressful conditions and its interspecific interactions Ó 2011 The Authors New Phytologist (2011) 1 New Phytologist Ó 2011 New Phytologist Trust www.newphytologist.com New 2 Research Phytologist (Brody, 1997; Augspurger, 2009; Devaux & Lande, 2010) then Flowering should be reduced during times of consistent extreme it could also be part of a larger plant strategy that incorporates temperatures and ⁄ or minimum soil moisture. We test this other functional traits. Flower production and maintenance as hypothesis by comparing the frequency of first flowering dates well as subsequent reproduction is resource-intensive (Ashman & (FFDs) across species with long-term records of air temperatures, Schoen, 1994; Obeso, 2002), which might tend to favor repro- precipitation, and soil moisture. Secondly, if environmental stress duction during times of low environmental stress. For example, is a determinant of flowering for a given species, species that high leaf tissue density is favored under conditions of low nutri- flower during the most stressful times should have traits that con- ent availability in grasslands and considered part of a broader fer resistance to environmental stress or low resource availability. low-nutrient strategy (Craine et al., 2001; Craine, 2009; Craine To test this hypothesis, we examined relationships between & Towne, 2010). Thus if nutrient availability varies seasonally, flowering time and average leaf tissue density – a proxy for stress species that flower during periods of low nutrient availability tolerance – for c. 400 species, as well as relationships over a might also have high leaf tissue density. Seasonal variation in smaller number of species with other functional traits such as drought could also generate links between plant functional traits physiological drought tolerance and photosynthetic rates that are and flowering phenology. For example, when stresses become associated with plant resource strategies. severe enough to constitute a disturbance (e.g. prolonged Lastly, to determine whether the timing of flowering contrib- drought), species with high-activity, rapid-turnover tissues would utes to the abundance of a species, we examined relationships be favored. For example, severe droughts that generate wide- between flowering time and abundance across three main ecolog- spread mortality across all species can favor annuals over perenni- ical contrasts at Konza: topography, fire, and grazing. At Konza als (Weaver, 1968). If the probability of drought varies Prairie, uplands have shallower soils than lowlands and species seasonally, times of typical low soil moisture could be more likely that are more physiologically drought-tolerant (Craine et al., to have species with traits that confer drought resistance, while 2011). We compared watersheds that are burned annually in the times after the drought could be associated with species that have spring with those that are infrequently burned because annual traits associated with disturbance, such as low leaf tissue density. spring burning might preferentially decrease the abundance of Ultimately, if flowering phenology is not neutral and is associ- early flowering species (Howe, 1994). Finally, we compared the ated with responses to environmental conditions and plant abundance of species with different flowering times in areas functional traits then flowering phenology should also be linked grazed by bison with those not grazed by bison. Although grazing to species abundance on a landscape (Willis et al., 2010). For decreases the abundance of C4 grasses and increases species rich- example, if environmental stress varies over the course of a grow- ness (Knapp et al., 1999; Collins & Smith, 2006), we do not ing season, species that flower during stressful times might be less know, for example, whether grazing increases the richness of spe- abundant, linking flowering time and abundance. Competition cies that flower late in the growing season as a consequence of for pollinator resources could in turn strengthen associations competitive release. between abundance and flowering time driven also by patterns of environmental stress. If competition for pollination resources is Materials and Methods an important associate of flowering time, then there might be fewer species that
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